Skip to main content

Advertisement

SpringerLink
Log in

The nutritional physiology of sharks

  • Reviews
  • Published:
Reviews in Fish Biology and Fisheries Aims and scope Submit manuscript

Abstract

Sharks compose one of the most diverse and abundant groups of consumers in the ocean. Consumption and digestion are essential processes for obtaining nutrients and energy necessary to meet a broad and variable range of metabolic demands. Despite years of studying prey capture behavior and feeding habits of sharks, there has been little exploration into the nutritional physiology of these animals. To fully understand the physiology of the digestive tract, it is critical to consider multiple facets, including the evolution of the system, feeding mechanisms, digestive morphology, digestive strategies, digestive biochemistry, and gastrointestinal microbiomes. In each of these categories, we make comparisons to what is currently known about teleost nutritional physiology, as well as what methodology is used, and describe how similar techniques can be used in shark research. We also identify knowledge gaps and provide suggestions to continue the progression of the field, ending with a summary of new directions that should be addressed in future studies regarding the nutritional physiology of sharks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Illustrations by R. Aidan Martin (2003)

Fig. 2

(Revised from Motta and Wilga 1995 by J.S. German)

Fig. 3

Images from Paig-Tran and Summers (2014), used with permission

Fig. 4

From Wilson and Castro (2011), used with permission

Fig. 5

Adapted from Jhaveri et al. 2015

Fig. 6

Images from Wilson and Castro (2011), used with permission

Fig. 7

Illustrations by A. Dingeldein. CT scan image reconstructions by S. Leigh

Fig. 8

Modified from German (2011)

Fig. 9
Fig. 10

Adapted from Jhaveri et al. (2015)

Similar content being viewed by others

References

  • Aldman G, Jonsson AC, Jensen J, Holmgren S (1989) Gastrin/CCK-like peptides in the spiny dogfish, squalus acanthias-concentrations and actions in the gut. Comp Biochem Physiol C-Pharmacol Toxicol Endocrinol 91(1):103–108

    Article  Google Scholar 

  • Anderson WG, McCabe C, Brandt C, Wood CM (2015) Examining urea flux across the intestine of the spiny dogfish, Squalus acanthias. Comp Biochem Physiol 181:71–78

    Article  CAS  Google Scholar 

  • Andrews PLR, Young JZ (1988) The effect of peptides on the motility of the stomach, intestine and rectum in the skate. Comp Biochem Physiol CB9:343–348

    Google Scholar 

  • Andrews PLR, Young JZ (1993) Gastric motility patterns for digestion and vomiting evoked by sympathetic nerve stimulation and 5-hydroxytryptamine in the dogfish Scyliorhinus canicula. Philos Trans R Soc Lond 342:363–380

    Article  CAS  Google Scholar 

  • Armstrong JB, Schindler DE (2011) Excess digestive capacity in predators reflects a life of feast and famine. Nature 476:84–87

    Article  CAS  PubMed  Google Scholar 

  • Baldridge H (1970) Sinking factors and average densities of Florida sharks as a function of liver buoyancy. Copeia 4:744–754

    Article  Google Scholar 

  • Ballantyne JS (2016) Metabolism of elasmobranchs (Jaws II). In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: internal processes. Elsevier, London

    Google Scholar 

  • Beckmann CL, Mitchell JG, Seuront L, Stone DA, Huveneers C (2013) Experimental evaluation of fatty acid profiles as a technique to determine dietary composition in benthic elasmobranchs. Physiol Biochem Zool 86:266–278

    Article  CAS  PubMed  Google Scholar 

  • Beckmann CL, Mitchell JG, Stone DA, Huveneers C (2014) Inter-tissue differences in fatty acid incorporation as a result of dietary oil manipulation in Port Jackson Sharks (Heterodontus portusjacksoni). Lipids 49(6):577–590

    Article  CAS  PubMed  Google Scholar 

  • Bernal D, Lowe CG (2016) Field studies of elasmobranch physiology. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: structure and interaction with environment. Elsevier, London

    Google Scholar 

  • Bertin L (1958) Appareil digestif. In: Grasse PP (ed) Traite de Zoologic, vol 13. Mason, Paris, pp 1248–1302

    Google Scholar 

  • Bethea DM, Hale L, Carlson JK, Cortés E, Manire CA, Gelsleichter J (2007) Geographic and ontogenetic variation in the diet and daily ration of the bonnethead shark, Sphyrna tiburo, from the eastern Gulf of Mexico. Mar Biol 152:1009–1020

    Article  Google Scholar 

  • Bethea DM, Carlson JK, Hollensead LD, Papastamatiou YP, Graham BS (2011) A comparison of the foraging ecology and bioenergetics of the early life-stages of two sympatric hammerhead sharks. Bull Mar Sci 87(4):873–889

    Article  Google Scholar 

  • Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic Press, New York, pp 280–352

    Google Scholar 

  • Bucking C (2016) Feeding and digestion in elasmobranchs: tying diet and physiology together. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: structure and interaction with environment. Elsevier, London

    Google Scholar 

  • Bush AC, Holland KH (2002) Food limitation in a nursery area: estimates of daily ration in juvenile scalloped hammerheads, Sphyrna lewini, in Kanéohe Bay, O’ahu. J Exp Mar Biol Ecol 278:157–178

    Article  Google Scholar 

  • Calduch-Giner JA, Sitja-Bodadilla A, Perez-Sanches J (2016) Gene expression profiling reveals functional specialization along the intestinal tract of a carnivorous teleostean fish (Dicentrarchus labrax). Front Physiol. doi:10.3389/fphys.2016.00359

    PubMed  PubMed Central  Google Scholar 

  • Camp AL, Brainerd EL (2014) Role of axial muscles in powering mouth expansion during suction feeding in largemouth bass (Micropterus salmoides). J Exp Biol 217(8):1333–1345

    Article  PubMed  Google Scholar 

  • Camp AL, Roberts TJ, Brainerd EL (2015) Swimming muscles power suction feeding in largemouth bass. Proc Natl Acad Sci USA 112(28):8690–8695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cant J, McBride B, Croom W Jr (1996) The regulation of intestinal metabolism and its impact on whole animal energetics. J Anim Sci 74:2541–2553

    Article  CAS  PubMed  Google Scholar 

  • Carlisle AB, Litvin SY, Madigan DJ, Lyons K, Bigman JS, Ibarra M, Bizzarro JJ (2017) Interactive effects of urea and lipid content confound stable isotope analysis in elasmobranch fishes. Can J Fish Aquat Sci 74(3):419–428

    Article  CAS  Google Scholar 

  • Castro L, Goncalves O, Mazan S, Tay B, Venkatesh B, Wilson J (2014) Recurrent gene loss correlates with the evolution of stomach phenotypes in gnathostome history. Proc R Soc B 281:2013–2669

    Google Scholar 

  • Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Delta N-15 and Delta C-13): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46(2):443–453

    Article  CAS  Google Scholar 

  • Caut S, Jowers MJ, Michel L, Lepoint G, Fisk AT (2013) Diet- and tissue-specific incorporation of isotopes in the shark Scyliorhinus stellaris, a North Sea mesopredator. Mar Ecol Prog Ser 492:185–198

    Article  CAS  Google Scholar 

  • Chatchavalvanich K, Marcos R, Poonpirom J, Thongpan A, Rocha E (2006) Histology of the digestive tract of the freshwater stingray Himantura signifer Compagno and Roberts, 1982 (Sharkii, Dasyatidae). Anat Embryol 211:507–518

    Article  PubMed  Google Scholar 

  • Choat JH, Clements KD (1998) Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol Syst 29:375–403

    Article  Google Scholar 

  • Churchill DA, Heithaus MR, Vaudo JJ, Grubbs RD, Gastrich K, Castro JI (2015) Trophic interactions of common elasmobranchs in deep-sea communities of the Gulf of Mexico revealed through stable isotope and stomach content analysis. Deep-Sea Res II 115:92–102

    Article  CAS  Google Scholar 

  • Clements KD, Raubenheimer D, Choat JH (2009) Nutritional ecology of marine herbivorous fishes: ten years on. Funct Ecol 23(1):79–92

    Article  Google Scholar 

  • Clements KD, Angert ER, Montgomery WL, Choat JH (2014) Intestinal microbiota in fishes: what’s known and what’s not. Mol Ecol 23:1891–1898

    Article  PubMed  Google Scholar 

  • Clements KD, German DP, Piche J, Tribollet A, Choat JH (2017) Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol J Linn Soc

  • Cnudde C, Moens T, Werbrouck E, Lepoint G, Van Gansbeke D, De Troch M (2015) Trophodynamics of estuarine intertidal harpacticoid copepods based on stable isotope composition and fatty acid profiles. Mar Ecol Prog Ser 524:225–239

    Article  CAS  Google Scholar 

  • Compagno L (2008) Pelagic shark diversity. In: Camhi MD, Pikitch EK (eds) Sharks of the open ocean: biology, fisheries and conservation. Blackwell, Oxford, pp 14–23

    Chapter  Google Scholar 

  • Corn KA, Farina SC, Brash J, Summers AP (2016) Modeling tooth-prey interactions in sharks: the importance of dynamic testing. R Soc Open Sci 3:160141. doi:10.1098/rsos.160141

    Article  PubMed  PubMed Central  Google Scholar 

  • Cortés E (1996) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to shark fishes. Can J Fish Aquat Sci 54:726–738

    Article  Google Scholar 

  • Cortés E, Gruber SH (1996) Gastric evacuation in the young lemon shark, Negaprion brevirostris, under field conditions. Environ Biol Fishes 35:205–212

    Article  Google Scholar 

  • Cortés E, Papastamatiou Y, Carlson J, Ferry-Graham L, Wetherbee B (2008) An overview of the feeding ecology and physiology of shark fishes. In: Cyrino J, Bureau D, Kapoor B (eds) Feeding and digestive functions in fishes. Science Publishers, New Hampshire

    Google Scholar 

  • Crane R, Boge G, Rigal A (1979) Isolation of brushborder membranes in vesivular form from the intestinal spiral valve of the small dogfish (Scyliorhinus canicula). Biochim Biophys Acta 554:264–267

    Article  CAS  PubMed  Google Scholar 

  • Dalerum F, Angerbjorn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658

    Article  CAS  PubMed  Google Scholar 

  • Day RD, Tibbetts IR, Secor SM (2014) Physiological responses to short-term fasting among herbivorous, omnivorous, and carnivorous fishes. J Comp Physiol B 184:297–512

    Article  Google Scholar 

  • Dennis CA, MacNeil MA, Rosati JY, Pitcher TE, Fisk AT (2010) Diet discrimination factors are inversely related to δ15N and δ13C values of food for fish under controlled conditions. Rapid Commun Mass Spectrom 24:3515–3520

    Article  CAS  PubMed  Google Scholar 

  • Di Santo V, Bennett WA (2011) Is post-feeding thermotaxis advantageous in shark fishes? J Fish Biol 78:195–207

    Article  PubMed  Google Scholar 

  • Diamond JM, Karasov WH (1987) Adaptive regulation of intestinal nutrient transporters. Proc Natl Acad Sci USA 84(8):2242–2245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dove ADM, Leisen J, Zhou M, Byrne JJ, Lim-Hing K, Webb HD, Gelbaum L, Viant MR, Kubanek J, Fernandez FM (2012) Biomarkers of whale shark health: a metabolomic approach. PLoS ONE. doi:10.1371/journal.pone.0049379

    Google Scholar 

  • Dowd WW, Wood CM, Kajimura M, Walsh PJ, Kültz D (2008) Natural feeding influences protein expression in the dogfish shark rectal gland: a proteomic analysis. Comp Biochem Physiol D Genomics Proteomics 3:118–127

    Article  PubMed  CAS  Google Scholar 

  • Fänge R, Grove D (1979) Digestion. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 8. Academic Press, New York, pp 161–260

    Google Scholar 

  • Fänge R, Lundblad G, Lind J, Slettengren K (1979) Chitinolytic enzymes in the digestive system of marine fishes. Mar Biol 53:317–321

    Article  Google Scholar 

  • Ferry-Graham LA, Lauder GV (2001) Aquatic prey capture in ray-finned fishes: a century of progress and new directions. J Morphol 248:99–119

    Article  CAS  PubMed  Google Scholar 

  • Frazetta TH, Prange CD (1987) Movements of cephalic components during feeding in some requiem sharks (Carcharhiniformes: Carcharhinidae). Copeia 1987:979–993

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Furuse M, Dockray GJ (1995) The regulation of gastrin-secretion in the chicken. Regul Pept 55(3):253–259

    Article  CAS  PubMed  Google Scholar 

  • Gajić A (2013) Comparative odontology of selachians (Chondricthyes: Sharkii): development and morphological characteristics of teeth. Presented at the 17th annual Symposium of Biology Students in Europe. Abstract

  • Gamboa-Delgado J, Canavate JP, Zerolo R, Le Vay L (2008) Natural carbon stable isotope ratios as indicators of the relative contribution of live and inert diets to growth in larval Senegalese sole (Solea senegalensis). Aquaculture 280(1–4):190–197

    Article  CAS  Google Scholar 

  • German DP (2011) Digestive efficiency. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment, vol 3. Academic Press, San Diego, pp 1596–1607

    Chapter  Google Scholar 

  • German DP, Miles RD (2010) Stable carbon and nitrogen incorporation in blood and fin tissue of the catfish Pterygoplichthys disjunctivus (Siluriformes, Loricariidae). Environ Biol Fishes 89:117–133

    Article  Google Scholar 

  • German DP, Horn MH, Gawlicka A (2004) Digestive enzyme activities in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Physiol Biochem Zool 77(5):789–804

    Article  CAS  PubMed  Google Scholar 

  • German DP, Nagle BC, Villeda JM, Ruiz AM, Thomson AW, Contreras S, Evans DH (2010a) Evolution of herbivory in a carnivorous clade of minnows (Teleostei: Cyprinidae): effects on gut size and digestive physiology. Physiol Biochem Zool 83(1):1–18

    Article  PubMed  Google Scholar 

  • German DP, Neuberger DT, Callahan MN, Lizardo NR, Evans DH (2010b) Feast to famine: the effects of food quality and quantity on the gut structure and function of a detritivorous catfish (Teleostei: Loricariidae). Comp Biochem Physiol A 155:281–293

    Article  CAS  Google Scholar 

  • German DP, Sung A, Jhaveri P, Agnihotri R (2015) More than one way to be an herbivore: convergent evolution of herbivory using different digestive strategies in prickleback fishes (family Stichaeidae). Zoology 118:161–170

    Article  PubMed  Google Scholar 

  • German DP*, Foti DM*, Heras J, Amerkhanian H, Lockwood BL (2016) Elevated gene copy number does not always explain elevated amylase activities in fishes. Physiol Biochem Zool 89:277–293

    Article  PubMed  Google Scholar 

  • Gidmark NJ, Taylor C, LoPresti E, Brainerd E (2015) Functional morphology of Durophagy in Black Carp, Mylopharyngodon piceus. J Morphol 276(12):1422–1432

    Article  PubMed  Google Scholar 

  • Givens C, Ransom B, Bano N, Hollibaugh J (2015) Comparison of the gut microbiomes of 12 bony fish and 3 shark species. Mar Ecol Prog Ser 518:209–223

    Article  Google Scholar 

  • Goldman KJ, Anderson SD, Latour RJ, Musick JA (2004) Homeothermy in adult salmon sharks, Lamna ditropis. Environ Biol Fishes 71:403–411

    Article  Google Scholar 

  • Goran A, Jonsson A, Jensen J, Holmgren S (1988) Gastrin/CCK-like peptides in the spiny dogfish, Squalus acanthias; concentrations and actions in the gut. Comp Biochem Phys 92(1):103–108

    Google Scholar 

  • Grove DJ, Campbell G (1979) The role of extrinsic and intrinsic nerves in the co-ordination of gut motility in the stomachless flatfish Rhombosolea tapirina and Ammotretis rostrata Guenther. Comp Biochem Physiol C 63(1):143–159

    Article  Google Scholar 

  • Guerreiro I, de Vareilles M, Pousao-Ferreira P, Rodrigues V, Dinis MT, Ribeiro L (2010) Effect of age-at-weaning on digestive capacity of white seabream (Diplodus sargus). Aquaculture 300(1–4):194–205

    Article  Google Scholar 

  • Halver JE (2002) The vitamins. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 61–141

    Google Scholar 

  • Hart HR, Evans AN, Gelsleichter J, Ahearn GA (2016) Molecular identification and functional characteristics of peptide transporters in the bonnethead shark (Sphyrna tiburo). J Comp Physiol B 186(7):855–866

    Article  CAS  PubMed  Google Scholar 

  • Hesslein RH, Hallard KA, Ramlal P (1993) Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Can J Fish Aquat Sci 50:2071–2076

    Article  CAS  Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188

    Article  Google Scholar 

  • Hogben CAM (1967) Response of the isolated dogfish gastric mucosa to histamine. Proc Soc of Exp Biol Med 124:890–893

    Article  CAS  Google Scholar 

  • Holmgren S, Nilsson S (1999) Digestive system. In: Hamlett WC (ed) Sharks, skates, and rays: the biology of shark fishes. The Johns Hopkins University Press, Baltimore, pp 144–173

    Google Scholar 

  • Holmgren S, Grimes D, Brayton P, Colwell R, Gruber S (1985) Vibrios as autochthonous flora of neritic sharks. Syst Appl Microbiol 6:221–226

    Article  Google Scholar 

  • Horn MH, Messer KS (1992) Fish guts as chemical reactors: a model of the alimentary canals of marine herbivorous fishes. Mar Biol 113:527–535

    Article  Google Scholar 

  • Hume I (2003) Nutrition of carnivorous marsupials. In: Jones M, Dickman C, Archer M (eds) Predators with pouches: the biology of carnivorous marsupial. CSIRO Publishing, Collingwood, Australia, pp 221–227

    Google Scholar 

  • Hume I (2005) Concepts of digestive efficiency. In: Starck J, Wang T (eds) Physiological ecological adaptations to feeding vertebrates. Science Publishers, Enfield, pp 43–58

    Google Scholar 

  • Hussey NE, Brush J, McCarthy ID, Fisk AT (2010) δ15N and δ13C diet—tissue discrimination factors for large sharks under semi-controlled conditions. Comp Biochem Physiol A 155:445–453

    Article  CAS  Google Scholar 

  • Iverson SJ, Frost KJ, Lang SLC (2002) Fat content and fatty acid composition of forage fish and invertebrates in Prince William Sound, Alaska: factors contributing to among and within species variability. Mar Ecol Prog Ser 241:161–181

    Article  CAS  Google Scholar 

  • Jackson S, Dubby DC, Jenkins JFG (1987) Gastric digestion in marine vertebrate predators: in vitro standards. Funct Ecol 1:287–291

    Article  Google Scholar 

  • Jeschke JM (2007) When carnivores are “full and lazy”. Oecologia 152(2):357–364

    Article  PubMed  Google Scholar 

  • Jhaveri P, Papastamatiou Y, German DP (2015) Digestive enzyme activities in the guts of bonnethead sharks (Sphyrna tiburo) provide insight into their digestive strategy and evidence for microbial digestion in their hindguts. Comp Biochem Physiol A 189:76–83

    Article  CAS  Google Scholar 

  • Johnsen AH, Jonson L, Rourke IJ, Rehfeld JF (1997) Sharks express separate cholecystokinin and gastrin genes. Proc Natl Acad Sci USA 94(19):10221–10226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones BC, Green GH (1977) Food and feeding of spiny dogfish (Squalus acanchias) in British Columbia waters. J Fish Res Board Can 43:2067–2078

    Google Scholar 

  • Kararli T (1995) Comparison of the gastrointestinal anatomy, physiology, and biochemistry of human and commonly used laboratory animals. Biopharm Drug Dispos 16:351–380

    Article  CAS  PubMed  Google Scholar 

  • Karasov WH (1992) Tests of the adaptive modulation hypothesis for dietary control of intestinal nutrient transport. Am J Physiol 263:R496–R502

    CAS  PubMed  Google Scholar 

  • Karasov WH, Diamond J (1983) Adaptive regulation of sugar and amino acid transport by vertebrate intestine. Am J Physiol 245:G443–G462

    CAS  PubMed  Google Scholar 

  • Karasov WH, Douglas AE (2013) Comparative and digestive physiology. Compr Physiol 3:741–783

    PubMed  PubMed Central  Google Scholar 

  • Karasov WH, Martinez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, Princeton

    Google Scholar 

  • Karsten AH, Rice CD (2004) c-Reactive protein levels as a biomarker of inflammation and stress in the Atlantic sharpnose shark (Rhizoprionodon terraenovae) from three southeastern USA estuaries. Mar Environ Res 58(2–5):747–751

    Article  CAS  PubMed  Google Scholar 

  • Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22

    Article  CAS  Google Scholar 

  • Kenaley CP, Lauder GV (2016) A biorobotic model of the suction-feeding system in largemouth bass: the roles of motor program speed and hyoid kinematics. J Exp Biol 219:2048–2059

    Article  PubMed  Google Scholar 

  • Kim SL, Martinez del Rio C, Casper D, Koch PL (2012) Isotopic incorporation rates for shark tissues from a long-term captive feeding study. J Exp Biol 215(14):2495–2500

    Article  PubMed  Google Scholar 

  • Kolmann MA, Welch K, Summers AP, Lovejoy NR (2016) Always chew your food: freshwater stingrays use mastication to process tough insect prey. Proc R Soc B Biol Sci 283:20161392. doi:10.1098/rspb.2016.1392

    Article  CAS  Google Scholar 

  • Konturek JW, Thor P, Maczka M, Stoll R, Domschke W, Konturek SJ (1994) Role of cholecystokinin in the control of gastric emptying and secretory response to a fatty meal in normal subjects and duodenal ulcer patients. Scand J Gastroenterol 29(7):583–590

    Article  CAS  PubMed  Google Scholar 

  • Kuz’mina V (1990) Characteristics of enzymes involved in membrane digestion in shark fishes. Zhur Evolyut Biokhim Fiziolog 26:161–166

    Google Scholar 

  • Laurence-Chasen JD, Jimenez YE, Knorlein BJ, and Brainerd EL (2016) Video Reconstruction of Moving Morphology (VROMM) for studies of suction feeding in ray-finned fishes. Conference: Annual Meeting of the Society-for-Integrative-and-Comparative-Biology (SICB). Integrative and Comparative Biology, 56(1): E321, Meeting Abstract: P2.175, Portland, OR

  • Lauzon HL, Perez-Sanchez T, Merrifield DL, Ringo E, Balcazar JL (2014) Probiotic applications in cold water fish species. Aquac Nutr Gut Health Probiotics Prebiotics 9:223–252

    Google Scholar 

  • LeBlanc J, Milani C, Savoy de Giori G, Sesma F, van Sinderen D, Ventura M (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 24:160–168

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Zhang Y, Hussey NE, Dai X (2015) Urea and lipid extraction treatment effects on δ15N and δ13C values in pelagic sharks. Rapid Commun Mass Spectrom 30:1–8

    Article  CAS  Google Scholar 

  • Lloyd KCK, Debas HT (1994) Peripheral regulation of gastric acid secretion. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Plenum Publishing Corporation, New York, pp 229–334

    Google Scholar 

  • Logan JM, Lutcavage ME (2010) Stable isotope dynamics in elasmobranch fishes. Hydrobiologia 644:231–244

    Article  CAS  Google Scholar 

  • Longo SJ, McGee MD, Oufiero CE, Waltzek TB, Wainwright PC (2016) Body ram, not suction, is the primary axis of suction-feeding diversity in spiny-rayed fishes. J Exp Biol 219(1):119–128

    Article  PubMed  Google Scholar 

  • Lujan NK, German DP, Winemiller KL (2011) Do wood grazing fishes partition their niche? Morphological and isotopic evidence for trophic segregation in Neotropical Loricariidae. Funct Ecol 25:1327–1338

    Article  Google Scholar 

  • Mara KR, Motta PJ, Martin AP, Hueter RE (2015) Constructional morphology within the head of hammerhead sharks (Sphyrnidae). J Morphol 276(5):526–539

    Article  PubMed  Google Scholar 

  • Martin RA (2003) Biology of sharks and rays. Illustrations. World Wide Web Publication, www.elasmo-research.org/copyright.htm

  • Martine A, Fuhrman F (1995) The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol Biochem Zool 28:18–34

    Google Scholar 

  • Martínez del Rio C, Carleton SA (2012) How fast and how faithful—the dynamics of isotopic incorporation into animal tissues. J Mamm 93:353–359

    Article  Google Scholar 

  • Martinez del Rio C, Wolf N (2005) Mass-balance models for animal isotopic ecology. In: Starck MA, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, New Hampshire, pp 141–174

    Google Scholar 

  • Martinez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111

    Article  Google Scholar 

  • McCosker JE (1987) The white shark, Carcharodon carcharias, has a warm stomach. Copeia 1987:195–197

    Article  Google Scholar 

  • Meyer CG, Holland KN (2012) Autonomous measurement of ingestion and digestion processes in free-swimming sharks. J Exp Biol 215:3681–3684

    Article  PubMed  Google Scholar 

  • Michelangeli F, Ruiz MC, Dominquez MG, Parthe V (1988) Mammalian like differentiation of gastric cells in the shark Hecanchus griseus. Cell Tissue Res 251:225–227

    Article  CAS  PubMed  Google Scholar 

  • Moro GV, Silva TSC, Zanon RB, Cyrino JEP (2016) Starch and lipid in diets for dourado Salminus brasiliensis (Cuvier 1816): growth, nutrient utilization and digestive enzymes. Aquac Nutr 22(4):890–898

    Article  CAS  Google Scholar 

  • Motta PJ, Wilga CAD (1995) Anatomy of the feeding apparatus of the lemon shark, Negaprion brevirostris. J Morphol 226:309–329

    Article  Google Scholar 

  • Motta PJ, Wilga CAD (2001) Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environ Biol Fish 60:131–156

    Article  Google Scholar 

  • Motta PJ, Hueter RE, Tricas TC, Summers AP, Huber DR, Lowry D, Mara KR, Matott MP, Whitenack LB, Wintzer AP (2008) Functional morphology of the feeding apparatus, feeding constraints, and suction performance in the nurse shark. J Morphol 269:1041–1055

    Article  PubMed  Google Scholar 

  • Motta PJ, Maslanka M, Hueter RE, Davis RL, de la Parra R, Mulvany SL, Habegger ML, Strother JA, Mara KR, Gardiner JM, Tyminski JP, Zeigler LD (2010) Feeding anatomy, filter-feeding rate, and diet of whale sharks, Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology 113:199–212

    Article  PubMed  Google Scholar 

  • Muller M, Osse JWM (1984) Hydrodynamics of suction feeding in fish. Trans Zool Soc Lond 37:51–135

    Article  Google Scholar 

  • Mulley JF, Hargreaves AD, Hegarty MJ, Heller RS, Swain MT (2014) Transcriptomic analysis of the lesser spotted catshark (Scyliorhinus canicula) pancreas, liver and brain reveals molecular level conservation of vertebrate pancreas function. BioMed Cent. doi:10.1186/1471-2164-15-1074

    Google Scholar 

  • Murphy KP, Crush L, Twomey M, McLaughlin PD, Mildenberger IC, Moore N, Bye J, O’Connor OJ, McSweeney SE, Shanahan F, Maher MM (2015) Model-based iterative reconstruction in CT enterography. AJR Am J Roentgenol 205(6):1173–1181

    Article  PubMed  Google Scholar 

  • Nakaya K (2001) White band on upper jaw of megamouth shark, Megachasma pelagios, and its presumed function (Lamniformes: Megachasmidae). Bull Fac Sci Hokkaido Univ Sapporo 52:125–129

    Google Scholar 

  • Nakaya K, Matsumoto R, Suda K (2008) Feeding strategy of the megamouth shark Megachasma pelagios (Lamniformes: Megachasmidae). J Fish Biol 73(1):17–34

    Article  Google Scholar 

  • Navarro-Garcia G, Aguilar-Pacheco R, Cordova-Vallejo B, Suarez-Ramirez J, Bolanos A (2000) Lipid composition of the liver oil of shark species from the Caribbean and gulf of California waters. J Food Compos Anal 13(5):791–798

    Article  CAS  Google Scholar 

  • Navia A, Mejia-Falla P, Giraldo A (2007) Feeding ecology of shark fishes in coastal waters of the Columbian Eastern Tropical Pacific. BMC Ecol 7:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41(11):1553–1573

    Article  Google Scholar 

  • Nelson JD (2004) Distribution and foraging ecology by Whale Sharks (Rhincodon typus) within Bahia de los Angeles, Baja California Norte, Mexico. M.Sc. Thesis. San Diego State University, CA, USA

  • Newsome SD, Fogel ML, Kelly L, Martinez del Rio C (2011) Contributions of direct incorporation from diet and microbial amino acids to protein synthesis in Nile tilapia. Funct Ecol 25(5):1051–1062

    Article  Google Scholar 

  • Newsome SD, Wolf N, Peters J, Fogel ML (2014) Amino acid δ13C analysis shows flexibility in the routing of dietary protein and lipids to the tissue of an omnivore. Integr Comp Biol 54(5):890–902

    Article  PubMed  Google Scholar 

  • Newsome SD, Sabat P, Wolf N, Rader JA, Martinez del Rio C (2015) Multi-tissue δ2H analysis reveals altitudinal migration and tissue-specific discrimination patterns in Cinclodes. Ecosphere 6(11):1–18

    Article  Google Scholar 

  • Newton K, Wraith J, Dickson K (2015) Digestive enzyme activities are higher in the shortfin mako shark, Isurus oxyrinchus, than in ectothermic sharks as a result of visceral endothermy. Fish Physiol Biochem 41:887–898

    Article  CAS  PubMed  Google Scholar 

  • Nielsen JM, Popp BN, Winder M (2015) Meta-analysis of amino acid stable nitrogen isotope ratios for estimating trophic position in marine organisms. Oecologia 178:631–642

    Article  PubMed  Google Scholar 

  • Oliver AS, Vigna SR (1996) CCK-X receptors in the endothermic mako shark (Isurus oxyrinchus). Gen Comp Endocrinol 102(1):61–73

    Article  CAS  PubMed  Google Scholar 

  • Olsson C, Holmgren S (2001) The control of gut motility. Comp Biochem Physiol A-Mol Integr Physiol 128(3):481–503

    Article  CAS  PubMed  Google Scholar 

  • Olsson C, Aldman G, Larsson A, Holmgren S (1999) Cholecystokinin affects gastric emptying and stomach motility in the rainbow trout Oncorhynchus mykiss. J Exp Biol 202(2):161–170

    CAS  PubMed  Google Scholar 

  • Paig-Tran EWM, Lowe C (2010) Elemental and energy assimilation in the round stingray, Urobatis halleri. Annu Meet Soc Integr Comp Biol 50(1):E227

    Google Scholar 

  • Paig-Tran EWM, Summers AP (2013) Comparison of the structure and composition of the branchial filters of suspension feeding sharks. Anat Rec 297(4):701–715

    Article  Google Scholar 

  • Paig-Tran EWM, Bizzarro JJ, Strother JA, Summers AP (2011) Bottles as models: predicting the effects of varying swimming speed and morphology on size selectivity and filtering efficiency in fishes. J Exp Biol 214:1643–1654

    Article  PubMed  Google Scholar 

  • Papastamatiou Y (2007) The potential influence of gastric acid secretion during fasting on digestion time in leopard sharks (Triakis semifasciata). Comp Biochem Physiol A 147:37–42

    Article  CAS  Google Scholar 

  • Papastamatiou YP, Lowe CG (2004) Postprandial response of gastric pH in leopard sharks (Triakis semifasciata) and its use to study foraging ecology. J Exp Biol 207(Pt2):225–232

    Article  PubMed  Google Scholar 

  • Papastamatiou Y, Lowe C (2005) Variations in gastric acid secretion during periods of fasting between two species of shark. Comp Biochem Physiol A 141:210–214

    Article  CAS  Google Scholar 

  • Papastamatiou Y, Purkis S, Holland K (2007) The response of gastric pH and motility to fasting and feeding in free-swimming blacktip reef sharks, Carcharhinus melanopterus. J Exp Mar Biol Ecol 345:129–140

    Article  CAS  Google Scholar 

  • Papastamatiou YP, Watanabe YY, Bradley D, Dee LE, Weng K, Lowe CG, Caselle JE (2015) Drivers of daily routines in an ectothermic marine predator: Hunt warm, rest warmer? PLoS ONE 10:e0127807

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parker TJ (1885) On the intestinal spiral valve in the genus Raja. Zool Soc Lond Trans 11:49–61

    Article  Google Scholar 

  • Pei-You G, Jun-Xia L, Feng-Li L, Liang-Ming Z, Hai-Zhu X, Yan-Bin S (2015) Retrospective comparison of computed tomography enterography and magnetic resonance enterography in diagnosing small intestine disease. J Pak Med Assoc 65(7):710–714

    PubMed  Google Scholar 

  • Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129(1):69–96

    Article  CAS  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Pethybridge H, Daley R, Virtue P, Nichols P (2010) Lipid composition and partitioning of deepwater chondrichthyans: inferences of feeding ecology and distribution. Mar Biol 157(6):1367–1384

    Article  CAS  Google Scholar 

  • Pinhal D, Shivji MS, Nachtigall PG, Chapman DD, Martins C (2012) A streamlined DNA tool for global identification of heavily exploited coastal shark species (genus Rhizoprionodon). PLoS ONE 7(4):e34797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecol. 83:703–718

    Article  Google Scholar 

  • Post DM, Layman CA, Arrinton DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analysis. Oecologia 152:179–189

    Article  PubMed  Google Scholar 

  • Qian X, Ba Y, Zhuang Q, Zhong G (2014) RNA-seq technology and its application in fish transcriptomics. OMICS 18(2):98–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reich KJ, Bjorndal KA, Bolten AB (2007) The ‘lost years’ of green turtles: using stable isotopes to study cryptic lifestages. Biol Let 3:712–714

    Article  Google Scholar 

  • Reich KJ, Bjorndal KA, Martinez del Rio C (2008) Effects of growth and tissue type on the kinetics of (13)C and (15)N incorporation in a rapidly growing ectotherm. Oecologia 155(4):651–663

    Article  PubMed  Google Scholar 

  • Ringo E, Zhou Z, Vecino JLG, Wadsworth S, Romero J, Krojdahl A, Olsen RE, Dimitroglou A, Foey A, Davies S, Owen M, Lauzon HL, Martinsen LL, De Schryver P, Bossier P, Perstad S, Merrifield DL (2016) Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquac Nutr 22(2):219–282

    Article  CAS  Google Scholar 

  • Ruan GL, Li Y, Gao ZX, Wang HL, Wang WM (2010) Molecular characterization of trypsinogens and development of trypsinogen gene expression and tryptic activities in grass carp (Ctenopharyngodon idellus) and topmouth culter (Culter alburnus). Comp Biochem Physiol B Biochem Mol Biol 155(1):77–85

    Article  PubMed  CAS  Google Scholar 

  • Sachs G, Prinz C, Loo D, Bamberg K, Besancon M, Shin JM (1994) Gastric acid secretion: activation and inhibition. Yale J Biol Med 67:81–95

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert ML (2015) Functional anatomy and physiology of gastric secretion. Curr Opin Gastroenterol 31(6):479–485

    Article  PubMed  Google Scholar 

  • Secor S, Taylor J, Grosell M (2012) Selected regulation of gastrointestinal acid-base secretion and tissue metabolism for the diamondback water snake and Burmese python. J Exp Biol 215:185–196

    Article  CAS  PubMed  Google Scholar 

  • Sepulveda CA, Kohin S, Chan C, Vetter R, Graham JB (2004) Movement patterns, depthpreferences, and stomach temperatures of free-swimming juvenile mako sharks, Isurus oxyrinchus, in the Southern California Bight. Mar Biol 145:191–199

    Article  Google Scholar 

  • Shamur E, Zilka M, Hassner T, China V, Liberzon A, Holzmen R (2016) Automated detection of feeding strikes by larval fish using continuous high-speed digital video: a novel method to extract quantitative data from fast, sparse kinematic events. J Exp Biol 219(11):1608–1617

    Article  PubMed  Google Scholar 

  • Sibly RM (1981) Strategies of digestion and defecation. In: Townsend CR, Callow P (eds) Physiological ecology: an evolutionary approach to resource use. Sinauer, Sunderland, pp 109–139

    Google Scholar 

  • Silverthorn D (ed) (2013) Human physiology: an integrated approach, vol 6. Pearson, Boston, p 699

    Google Scholar 

  • Sims D, Davies S, Bone Q (1996) Gastric emptying rate and return of appetite in lesser spotted dogfish, Scyliorhinus canicula. J Mar Biol. Assn UK 76:479–491

    Article  Google Scholar 

  • Sims D, Wearmouth VJ, Southall EJ, Hill JM, Moore P, Rawlinson K, Hutchinson N, Budd GC, Righton D, Metcalfe JD, Nash JP, Morritt D (2006) Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration in a benthic shark. J Anim Ecol 75:176–190

    Article  PubMed  Google Scholar 

  • Smith MM, Johanson Z, Underwood C, Diekwisch TGH (2013) Pattern formation in development of chondrichthyan dentitions: a review of an evolutionary model. Hist Biol Int J Paleobiol 25(2):127–142

    Google Scholar 

  • Sole M, Lobera G, Aljinovic B, Rios J, de la Parra LMG, Maynou F, Cartes JE (2008) Cholinesterases activities and lipid peroxidation levels in muscle from shelf and slope dwelling fish from the NW Mediterranean: its potential use in pollution monitoring. Sci Total Environ 402:306–317

    Article  CAS  PubMed  Google Scholar 

  • Sole M, Anto M, Baena M, Carrasson M, Cartes JE, Maynou F (2010) Hepatic biomarkers of xenobiotic metabolism in eighteen marine fish from NW Mediterranean shelf and slope waters in relation to some of their biological and ecological variables. Mar Environ Res 70(2):181–188

    Article  CAS  PubMed  Google Scholar 

  • Song Z, Wang J, Qiao H, Li P, Zhang L, Xia B (2016) Ontogenetic changes in digestive enzyme activities and the amino acid profile of starry flounder Platichthys stellatus. Chin J Oceanol Limnol 34(5):1013–1024

    Article  CAS  Google Scholar 

  • Sullam KE, Dalton CM, Russell JA, Kilham SS, El-Sabaawi R, German DP, Flecker AS (2014) Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies. Oecologia 177(1):245–257

    Article  PubMed  Google Scholar 

  • Summers AP, Hayes M (2016) CT scans. Retrieved from www.osf.io/ecmz4

  • Suzuki KW, Kasai A, Nakayama K, Tanaka M (2005) Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Can J Fish Aquat Sci 62(3):671–678

    Article  Google Scholar 

  • Suzuki T, Kakizaki H, Ikeda M, Matsumiya M (2014) Molecular cloning of the novel chitinase gene from blue shark (Prionace glauca; Chondrichthyes) stomach. J Chitin Chitosan Sci 2(2):143–148

    Article  Google Scholar 

  • Teles OA (2012) Nutrition and health of aquaculture fish. J Fish Dis 35:83–108

    Article  CAS  Google Scholar 

  • Trueman CN, McGill RAR, Guyard PH (2005) The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Spectrom 19(22):3239–3247

    Article  CAS  PubMed  Google Scholar 

  • Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM, Swann JB, Ohta Y, Flajnik MF, Sutoh Y, Kasahara M, Hoon S, Gangu V, Roy SW, Irimia M, Korzh V, Kondrychyn I, Lim ZW, Tay BH, Tohari S, Kong KW, Ho S, Lorente-Galdos B, Quilez J, Marques-Bonet T, Raney BJ, Ingham PW, Tay A, Hillier LW, Minx P, Boehm T, Wilson RK, Brenner S, Warren WC (2014) Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viana TP, Inacio AF, de Albuquerque C, Linde-Arias AR (2008) Biomarkers in a shark species to monitor marine pollution: Effects of biological parameters on the reliability of the assessment. Mar Environ Res 66:171

    Google Scholar 

  • Vigna S (1983) Evolution of endocrine regulation of gastrointestinal function in lower vertebrates. Am Zool 23:729–738

    Article  CAS  Google Scholar 

  • Vollaire Y, Banas D, Marielle T, Roche H (2007) Stable isotope variability in tissues of the Eurasian perch Perca fluviatilis. Comp Biochem Physiol A-Mol Integr Physiol 148(3):504–509

    Article  PubMed  CAS  Google Scholar 

  • Wainwright D, Lauder GV (2016) Three-dimensional analysis of scale morphology in bluegill sunfish, Lepomis macrochirus. Zoology 119(3):182–195

    Article  PubMed  Google Scholar 

  • Weidel BC, Carpenter SR, Kitchell JF, Vander Zanden MJ (2011) Rates and components of carbon turnover in fish muscle: insights from bioenergetics models and a whole-lake 13C addition. Can J Fish Aquat Sci 68:387–399

    Article  CAS  Google Scholar 

  • Wetherbee B, Gruber S (1993) Absorption efficiency of the lemon shark negaprion brevirostris at varying rates of energy intake. Copeia 2:416–425

    Article  Google Scholar 

  • Wetherbee B, Gruber S, Ramsey A (1987) X-radiographic observations of food passage through digestive tracts of lemon sharks. Trans Am Fish Soc 116:763–767

    Article  Google Scholar 

  • Wetherbee BM, Gruber SH, Cortés E (1990) Diet, feeding habits, digestion, and consumption in sharks, with special reference to the lemon shark, Negaprion brevirostris. NOAA Tech Rep NMFS 90:29–47

    Google Scholar 

  • Whitehead A, Galvez F, Zhang S, Williams LM, Oleksiak MF (2011) Functional genomics of physiological plasticity and local adaptation in killfish. J Hered 102(5):499–511

    Article  PubMed  Google Scholar 

  • Wilga CD, Ferry LA (2016) Functional anatomy and biomechanics of feeding in elasmobranchs. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: internal processes. Elsevier, London

    Google Scholar 

  • Wilga CD, Motta PJ (2000) Durophagy in sharks: Feeding mechanics of the hammerhead Sphyrna tiburo. J Exp Biol 201:1345–1358

    Google Scholar 

  • Wilson J, Castro L (2011) Morphological diversity of the gastrointestinal tract in fishes. Fish Physiol 30:1–55

    Google Scholar 

  • Wolesensky W, Logan JD (2006) Chemical reactor models of digestion modulation. In: Burk AR (ed) Focus on ecology research, pp 197–247

  • Wolf N, Newsome SD, Fogel ML, Martinez del Rio C (2012) An experimental exploration of the incorporation of hydrogen isotopes from dietary tissues into avian tissues. J Exp Biol 215:1915–1922

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Kajimura M, Bucking C, Walsh PJ (2007) Osmoregulation, ionoregulation and acid-base regulation by the gastrointestinal tract after feeding in the shark (Squalus acanthias). J Exp Biol 210:1335–1349

    Article  CAS  PubMed  Google Scholar 

  • Wu JL, Zhang JL, Du XX, Shen YJ, Lao X, Zhang ML, Chen LQ, Du ZY (2015) Evaluation of the distribution of adipose tissues in fish using magnetic resonance imaging (MRI). Aquaculture 448:112–122

    Article  CAS  Google Scholar 

  • Wyffels J, King BL, Vincent J, Chen C, Wu CH, Polson SW (2014) SkateBase, an shark genome project and collection of molecular resources for chondrichthyan fishes. F1000 Research, v1; ref status: indexed, http://f1000r.es/445

  • Zarkasi KZ, Taylor RS, Abell GC, Tamplin ML, Glencross BD, Bowman JP (2016) Atlantic salmon (Salmo salar L.) gastrointestinal microbial community dynamics in relation to digesta properties and diet. Microb Ecol 71(3):589–603

    Article  CAS  PubMed  Google Scholar 

  • Zuanon JAS, Pezzato AC, Ducatti C, Barros MM, Pezzato LE, Passos JRS (2007) Muscle delta C-13 change in nile tilapia (Oreochromis niloticus) fingerlings fed lants grain-based diets. Comp Biochem Physiol A-Mol Integr Physiol 147(3):761–765

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the comparative physiology group at UCI for providing guidance and advice, particularly J. Heras, B. Wehrle, and A. Frederick. J. German and A. Dingeldein helped with image creation and analysis. CT scanning facility and assistance provided by A. Summers and the University of Washington at Friday Harbor Laboratories.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, 92697, USA

    Samantha C. Leigh & Donovan P. German

  2. Marine Sciences Program, Department of Biological Science, Florida International University, 3000 NE 151st St, Miami, FL, 33181, USA

    Yannis Papastamatiou

Authors
  1. Samantha C. Leigh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yannis Papastamatiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Donovan P. German
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Samantha C. Leigh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Leigh, S.C., Papastamatiou, Y. & German, D.P. The nutritional physiology of sharks. Rev Fish Biol Fisheries 27, 561–585 (2017). https://doi.org/10.1007/s11160-017-9481-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11160-017-9481-2

Keywords

Search

Navigation